Abstract: Aspects of an entrenched constitution that were essential parts of founding compromises, and justified as necessary when a constitution was first adopted, may become less justifiable over time. Is this the case with respect to the structure of the United States Senate? The US Senate is hardwired in the Constitution to consist of an equal number of Senators from each state—the smallest of which currently has about 585,000 residents, and the largest of which has about 39.29 million. As this essay explains, over time, as population inequalities among states have grown larger, so too has the disproportionate voting power of smaller-population states in the national Senate. As a result of the ‘one-person, one-vote’ decisions of the 1960s that applied to both houses of state legislatures, each state legislature now is arguably more representative of its state population than the US Congress is of the US population. The ‘democratic deficit’ of the Senate, compared to state legislative bodies, also affects presidential (as compared to gubernatorial) elections. When founding compromises deeply entrenched in a constitution develop harder-to-justify consequences, should constitutional interpretation change responsively? Possible implications of the ‘democratic’ difference between the national and the state legislatures for US federalism doctrine are explored, especially with respect to the ‘pre-emption’ doctrine. Finally, the essay briefly considers the possibilities of federalism for addressing longer term issues of representation, polarisation and sustaining a single nation.